QUICK SEARCH:   [advanced] Author: Keyword(s):
Home     Help     Feedback     Subscriptions     Archive     Search     Table of Contents

First published online August 8, 2008
Journal of Experimental Biology 211, 2647-2657 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.019273

This Article Summary Full Text Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Related articles in JEB Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Voigt, D. Articles by Gorb, S. Search for Related Content PubMed PubMed Citation Articles by Voigt, D. Articles by Gorb, S. Social Bookmarking                         What's this?

An insect trap as habitat: cohesion-failure mechanism prevents adhesion of Pameridea roridulae bugs to the sticky surface of the plant Roridula gorgonias

Dagmar Voigt^* and Stanislav Gorb

Evolutionary Biomaterials Group, Department of Thin-Films and Biological Systems, Max-Planck Institute for Metals Research, Heisenbergstraße 03, D-70569 Stuttgart, Germany

View larger version (14K): [in this window] [in a new window]   Fig. 1. Diagram of hypothetical interactions between the plant adhesive and the insect cuticle. (A) Cuticle with no anti-adhesive properties. (B) Epicuticle, non-wettable by the Roridula adhesive owing to the specific chemistry of the surface. (C) Microstructure preventing adhesion. (D) Easy-to-break solid layer preventing strong bonding of adhesive to the epicuticle. (E) Fluid layer providing cohesion failure. Black area, solid insect surface; dotted area, plant adhesive fluid; hatched area, plant surface; white area, fluid layer. Arrows indicate the direction of movement of the insect surface.

View larger version (5K): [in this window] [in a new window]   Fig. 2. Experimental design for adhesion force measurements of single droplets of the adhesive secretion in tentacle-shaped trichomes. The living or dead test insect (TI), with its dorsal side attached to a glass slide (GS) with a droplet of beeswax (WD), is mounted on a horizontal holder (HO). A tentacle-shaped glandular trichome (GT) with a distinct terminal droplet of adhesive secretion is attached to a piece of double-sided carbon tape (DC) adhering firmly to a force sensor (FS). The sensor with the trichome was moved down using a motorized micromanipulator until contact between the droplet and the test surface (insect, glass) occurred at a load of approximately 50 µN, and then the sensor with the trichome was pulled up. The time–force sensor signal was recorded and processed further in a computer (PC).

View larger version (127K): [in this window] [in a new window]   Fig. 3. (A–D) Digital images of Pameridea roridulae walking on leaves of Roridula gorgonias covered with glandular trichomes: (A) adult P. roridulae; (B) fifth-instar nymph; (C) first-instar larva; (D) adult sucking on a stuck cricket. (E–G) Prey insects adhering to the secretion: (E,G) ventrally trapped Drosophila sp.; (F) laterally trapped fly of the family Sciaridae. (H) Two images of adhesive secretion filaments pulled away with a needle from the tip of tentacle-shaped trichomes; scale units: millimetres.

View larger version (144K): [in this window] [in a new window]   Fig. 4. Cryo-SEM micrographs of glandular trichomes and their adhesive secretion in Roridula gorgonias. (A) Leaf margin bearing capitate trichomes of varying lengths with glandular secretion droplets, partly adhering to the metal surface of the sample holder and partly transformed into fluid filaments. (B) Short capitate trichomes against a background of multicellular bases of tentacle-shaped trichomes, and a layer of glandular secretion on the leaf epidermis. (C) Short capitate trichome on the abaxial leaf lamina consisting of a large spherical, glandular head, covered by adhesive secretion, and a multicellular stalk. (D) Detail of the surface of the glandular secretion released by short capitate trichomes. Note the uneven profile of the fluid surface. (E) The tip of a long, tentacle-shaped trichome releasing an ovoid secretion droplet with a smooth surface. Note that the secretion runs down along the stalk of the trichome. (F) Detail of the fractured multicellular stalk of a tentacle-shaped trichome covered with a thick layer of glandular secretion. ff, fluid filaments; gs, glandular secretion; tb, base of the tentacle-shaped trichome; mt, multicellular trichome. Scale bars, 500 µm (A); 100 µm (B,E); 20 µm (C,D,F).

View larger version (71K): [in this window] [in a new window]   Fig. 5. Cryo-SEM micrographs of the glandular tips of tentacle-shaped trichomes in Roridula gorgonias after different treatments. (A) Intact voluminous, ovoid droplet of adhesive secretion after washing with aqua millipore. (B,C) Terminal gland covered with a fragmented layer of adhesive secretion after rinsing with ethanol. (D,E) Collapsed terminal gland with adhering fibrous formations of adhesive secretion residues after washing with chloroform. (F,G) Terminal gland after washing with acetone: the adhesive secretion is totally removed, and the glandular opening is clearly visible on the tip. Scale bars, 25 µm (A,B,D,F,G); 10 µm (C,E).

View larger version (191K): [in this window] [in a new window]   Fig. 6. Cryo-SEM micrographs showing the adhesive secretion of Roridula gorgonias in contact with (A–C) the surface of the mirid bug Pameridea roridulae, (D–F) the fly Calliphora vicina and (G–I) epoxy resin Spurr coated with gold–palladium. (A,B) Secretion droplet on the ventral abdomen of P. roridulae. (C) A spherical secretion droplet adhering to bristles in P. roridulae. (D,E) Secretion droplet on the ventral surface of the abdomen of C. vicina. (F) Adhesive secretion on setae of C. vicina. (G,H). Adhesive secretion in contact with a metallized Spurr surface. (I) Numerous micro-droplets left after the removal of a secretion droplet (G,H) from the metallized Spurr surface. Arrows point to secretion droplets on the insect surface. Scale bars, 200 µm (A,D,G); 50 µm (B,E,F,H,I); 5 µm (C).

View larger version (14K): [in this window] [in a new window]   Fig. 7. (A) Box-and-whisker diagram of the adhesion force of single adhesive droplets in the tentacle-shaped trichomes of Roridula gorgonias, measured on different surfaces. The ends of the boxes define the 25th and 75th percentiles, with a line at the median and error bars defining the 10th and 19th percentiles. Arrows point to areas of substrates where force was measured. (B) Statistical differences between surfaces (Kruskal–Wallis one-way ANOVA on ranks, H5,119=25.317, P0.001 and Tukey test, P<0.05).

View larger version (15K): [in this window] [in a new window]   Fig. 8. Examples of force–distance curves obtained by adhering trichomes of Roridula gorgonias to the ventral surface of the abdominal cuticle of living insects. The curves were used to calculate the work (shaded areas) that had to be applied to retract the adhering trichomes to a distance of 1.5 mm. (A) Data obtained on Pameridea roridulae. (B) Data obtained on Calliphora vicina.

View larger version (147K): [in this window] [in a new window]   Fig. 9. Phase-contrast light-microscopy images of prints left after pressing an insect cuticle against a glass slide. (A–D) Prints of adult Pameridea roridulae showing considerable fluid residues from (A) the head of a living insect, (B) the abdomen of a living insect, (C) the wing of a living insect and (D) the wing of a dry insect. (E,F) Prints of living (E) adult Calliphora vicina wing and (F) abdomen, showing only scattered micropatterns of grease residues. The arrow points to a broken bug seta leaving traces of parallel oriented lines corresponding to its helical surface texture. Scale bar, 50 µm.

View larger version (199K): [in this window] [in a new window]   Fig. 10. Cryo-SEM micrographs of the leg cuticle of different insects. (A–F) Adult Pameridea roridulae bug. Cross-fractures of (A) a freshly killed and (B) a dead, dry mirid bug show a distinct layer of epicuticular grease. (C) The layer disappears after washing bugs in cold chloroform. Top views of cuticle in (D) a freshly killed, (E) a dead, dry and (F) a dry, chloroform-washed mirid bug. (G–I) Adult Calliphora vicina fly. Cross-fractures of (G) a freshly killed, (H) dead, dry and (I) a dry, chloroform-washed C. vicina. All preparations are missing a distinct epicuticular grease layer. The arrowheads indicate epicuticular grease layer; m, microtrichia; ep, epicuticle; ex, exocuticle; en, endocuticle. Scale bars, 2 µm.

View larger version (11K): [in this window] [in a new window]   Fig. 11. Diagram demonstrating hypothetical interactions between the adhesive fluid of the plant Roridula gorgonias and the insect cuticle. (A) A thin greasy film, consisting of many single patches of tiny droplets, as demonstrated for the fly Calliphora vicina. Such a surface offers islands of solid cuticle as contact sites for the plant adhesive fluid. (B) A thick grease layer in the cuticle of the mirid bug Pameridea roridulae preventing the adhesion of the plant secretion by means of cohesion failure.

CiteULike

Complore

Connotea

Del.icio.us

Digg

Reddit

Technorati

Twitter